Phenotyping from lab to field – tomato lines screened for heat stress using Fv/Fm maintain high fruit yield during thermal stress in the field
Damodar Poudyal
A D , Eva Rosenqvist B and Carl-Otto Ottosen C
+ Author Affiliations
- Author Affiliations
A Research-for-Development Department, SEAN Seed Service Centre Limited, Chandragiri-7, Kathmandu, Nepal.
B Department of Plant and Environmental Sciences, University of Copenhagen, Højbakkegård Allé 9, 2630 Taastrup, Denmark.
C Department of Food Science, Aarhus University, Kirstinebjergvej 10, DK-5792 Årslev, Denmark.
D Corresponding author. Email: damodarpoudyal@gmail.com
Functional Plant Biology 46(1) 44-55 https://doi.org/10.1071/FP17317
Submitted: 12 November 2017 Accepted: 15 August 2018 Published: 15 October 2018
Abstract
This study aimed to phenotype young tomato (Solanum lycopersicum L.) plants for heat tolerance by measuring Fv/Fm after short-term heat treatments in climate chambers and selected sensitive (low Fv/Fm) and tolerant (high Fv/Fm) cultivars to investigate their in-field performance. Twenty-eight genotypes were phenotyped at 40 : 28°C for 2 days in climate chambers. A second screening (four high Fv/Fm and four low Fv/Fm genotypes) was conducted for 4 days at 38 : 28°C, followed by 5 days’ recovery (26 : 20°C). The tolerant genotypes maintained high net photosynthesis (PN) and increased stomatal conductance (gs) at 38°C, allowing better leaf cooling. Sensitive genotypes had lower Fv/Fm and PN at 38°C, and gs increased less than in the tolerant group, reducing leaf cooling. Under controlled conditions, all eight genotypes had the same plant size and pollen viability, but after heat stress, plant size and pollen viability reduced dramatically in the sensitive group. Two tolerant and two sensitive genotypes were grown in the field during a heat wave (38 : 26°C). Tolerant genotypes accumulated more biomass, had a lower heat injury index and higher fruit yield. To our knowledge, this is the first time screening for heat tolerance by Fv/Fm in climate chambers was verified by a field trial under natural heat stress. The differences after heat stress in controlled environments were comparable to those in yield between tolerant and sensitive groups under heat stress in the field. The results suggest that Fv/Fm is effective for early detection of heat tolerance, and screening seedlings for heat sensitivity can speed crop improvement.
Additional keywords: agronomic traits, chlorophyll fluorescence, dry weight, heat injury, leaf temperature, physiological markers.
References
Asseng S, Turner NC, Ray JD, Keating BA (2002) A simulation analysis that predicts the influence of physiological traits on the potential yield of wheat. European Journal of Agronomy 17, 123–141.| A simulation analysis that predicts the influence of physiological traits on the potential yield of wheat.Crossref | GoogleScholarGoogle Scholar |
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89–113.
| Chlorophyll fluorescence: a probe of photosynthesis in vivo.Crossref | GoogleScholarGoogle Scholar |
Baker NR, Rosenqvist E (2004) Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities. Journal of Experimental Botany 55, 1607–1621.
| Applications of chlorophyll fluorescence can improve crop production strategies: an examination of future possibilities.Crossref | GoogleScholarGoogle Scholar |
Berry J, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31, 491–543.
| Photosynthetic response and adaptation to temperature in higher plants.Crossref | GoogleScholarGoogle Scholar |
Bita CE, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Frontiers in Plant Science 4, 273
| Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops.Crossref | GoogleScholarGoogle Scholar |
Brestic M, Zivcak M (2013) PSII fluorescence techniques for measurement of drought and high temperature stress signal in crop plants: protocols and applications. In ‘Molecular stress physiology of plants’. (Eds G Rout, A Das) pp. 87–131. (Springer: New Delhi, India)
Brestic M, Zivcak M, Kalaji HM, Carpentier R, Allakhverdiev SI (2012) Photosystem II thermostability in situ: environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L. Plant Physiology and Biochemistry 57, 93–105.
| Photosystem II thermostability in situ: environmentally induced acclimation and genotype-specific reactions in Triticum aestivum L.Crossref | GoogleScholarGoogle Scholar |
Brestic M, Zivcak M, Kunderlikova K, Allakhverdiev SI (2016) High temperature specifically affects the photoprotective responses of chlorophyll b-deficient wheat mutant lines. Photosynthesis Research 130, 251–266.
| High temperature specifically affects the photoprotective responses of chlorophyll b-deficient wheat mutant lines.Crossref | GoogleScholarGoogle Scholar |
Brestic M, Zivcak M, Hauptvogel P, Misheva S, Kocheva K, Yang X, Li X, Allakhverdiev SI (2018) Wheat plant selection for high yields entailed improvement of leaf anatomical and biochemical traits including tolerance to non-optimal temperature conditions. Photosynthesis Research 136, 245–255.
| Wheat plant selection for high yields entailed improvement of leaf anatomical and biochemical traits including tolerance to non-optimal temperature conditions.Crossref | GoogleScholarGoogle Scholar |
Čajánek M, Štroch M, Lachetova I, Kalina J, Spunda V (1998) Characterization of the photosystem II inactivation of heat-stressed barley leaves as monitored by the various parameters of chlorophyll a fluorescence and delayed fluorescence. Journal of Photochemistry and Photobiology. B, Biology 47, 39–45.
| Characterization of the photosystem II inactivation of heat-stressed barley leaves as monitored by the various parameters of chlorophyll a fluorescence and delayed fluorescence.Crossref | GoogleScholarGoogle Scholar |
Camejo D, Rodríguez P, Morales MA, Dell’Amico JM, Torrecillas A, Alarcón JJ (2005) High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. Journal of Plant Physiology 162, 281–289.
| High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility.Crossref | GoogleScholarGoogle Scholar |
Camejo D, Jiménez A, Alarcón JJ, Torres W, Gómez JM, Sevilla F (2006) Changes in photosynthetic parameters and antioxidant activities following heat-shock treatment in tomato plants. Functional Plant Biology 33, 177–187.
| Changes in photosynthetic parameters and antioxidant activities following heat-shock treatment in tomato plants.Crossref | GoogleScholarGoogle Scholar |
Dafni A, Firmage D (2000) Pollen viability and longevity: practical, ecological and evolutionary implications. Plant Systematics and Evolution 222, 113–132.
| Pollen viability and longevity: practical, ecological and evolutionary implications.Crossref | GoogleScholarGoogle Scholar |
Guilioni L, Wery J, Tardieu F (1997) Heat stress-induced abortion of buds and flowers in pea: is sensitivity linked to organ age or to relations between reproductive organs? Annals of Botany 80, 159–168.
| Heat stress-induced abortion of buds and flowers in pea: is sensitivity linked to organ age or to relations between reproductive organs?Crossref | GoogleScholarGoogle Scholar |
Haque MS, Kjaer KH, Rosenqvist E, Sharma DK, Ottosen C-O (2014) Heat stress and recovery of photosystem II efficiency in wheat (Triticum aestivum L.) cultivars acclimated to different growth temperatures. Environmental and Experimental Botany 99, 1–8.
| Heat stress and recovery of photosystem II efficiency in wheat (Triticum aestivum L.) cultivars acclimated to different growth temperatures.Crossref | GoogleScholarGoogle Scholar |
Heckathorn SA, Coleman JS, Hallberg RL (1997) Recovery of net CO2 assimilation after heat stress is correlated with recovery of oxygen-evolving-complex proteins in Zea mays L. Photosynthetica 34, 13–20.
| Recovery of net CO2 assimilation after heat stress is correlated with recovery of oxygen-evolving-complex proteins in Zea mays L.Crossref | GoogleScholarGoogle Scholar |
Hong B, Ma C, Yang Y, Wang T, Yamaguchi-Shinozaki K, Gao J (2009) Over-expression of AtDREB1A in chrysanthemum enhances tolerance to heat stress. Plant Molecular Biology 70, 231–240.
| Over-expression of AtDREB1A in chrysanthemum enhances tolerance to heat stress.Crossref | GoogleScholarGoogle Scholar |
Ismail AM, Hall AE (1999) Reproductive-stage heat tolerance, leaf membrane thermostability and plant morphology in cowpea. Crop Science 39, 1762–1768.
| Reproductive-stage heat tolerance, leaf membrane thermostability and plant morphology in cowpea.Crossref | GoogleScholarGoogle Scholar |
Jedmowski C, Brüggemann W (2015) Imaging of fast chlorophyll fluorescence induction curve (OJIP) parameters, applied in a screening study with wild barley (Hordeum spontaneum) genotypes under heat stress. Journal of Photochemistry and Photobiology. B, Biology 151, 153–160.
| Imaging of fast chlorophyll fluorescence induction curve (OJIP) parameters, applied in a screening study with wild barley (Hordeum spontaneum) genotypes under heat stress.Crossref | GoogleScholarGoogle Scholar |
Karim MA, Fracheboud Y, Stamp P (1999) Photosynthetic activity of developing leaves of Zea mays is less affected by heat stress than that of developed leaves. Physiologia Plantarum 105, 685–693.
| Photosynthetic activity of developing leaves of Zea mays is less affected by heat stress than that of developed leaves.Crossref | GoogleScholarGoogle Scholar |
KC BR, Gurung S (2016) Study of solar energy potential using CMP6 Pyranometer at Nepalgunj. Journal of Advanced Academic Research 3, 51–58.
| Study of solar energy potential using CMP6 Pyranometer at Nepalgunj.Crossref | GoogleScholarGoogle Scholar |
Lu C-M, Zhang J-H (2000) Heat-induced multiple effects on PSII in wheat plants. Journal of Plant Physiology 156, 259–265.
| Heat-induced multiple effects on PSII in wheat plants.Crossref | GoogleScholarGoogle Scholar |
Nath K, Jajoo A, Poudyal RS, Timilsina R, Park YS, Aro E-M, Nam HG, Lee C-H (2013) Towards a critical understanding of the photosystem II repair mechanism and its regulation during stress conditions. FEBS Letters 587, 3372–3381.
| Towards a critical understanding of the photosystem II repair mechanism and its regulation during stress conditions.Crossref | GoogleScholarGoogle Scholar |
Perez-Alfocea F, Balibrea ME, Cruz AS, Estan MT (1996) Agronomical and physiological characterization of salinity tolerance in a commercial tomato hybrid. Plant and Soil 180, 251–257.
| Agronomical and physiological characterization of salinity tolerance in a commercial tomato hybrid.Crossref | GoogleScholarGoogle Scholar |
Poudyal D, Akash M, Khatri L, Shrestha DS, Uptmoor R (2017) Solanum habrochaites introgression line grafted as rootstock in cultivated tomato maintains growth and improves yield under cold and drought stresses. Journal of Crop Improvement 31, 589–607.
| Solanum habrochaites introgression line grafted as rootstock in cultivated tomato maintains growth and improves yield under cold and drought stresses.Crossref | GoogleScholarGoogle Scholar |
Pressman E, Peet MM, Pharr DM (2002) The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrate concentration in the developing anthers. Annals of Botany 90, 631–636.
| The effect of heat stress on tomato pollen characteristics is associated with changes in carbohydrate concentration in the developing anthers.Crossref | GoogleScholarGoogle Scholar |
Pressman E, Harel D, Zamski E, Shaked R, Althan L, Rosenfeld K, Firon N (2006) The effect of high temperatures on the expression and activity of sucrose-cleaving enzymes during tomato (Lycopersicon esculentum) anther development. The Journal of Horticultural Science & Biotechnology 81, 341–348.
| The effect of high temperatures on the expression and activity of sucrose-cleaving enzymes during tomato (Lycopersicon esculentum) anther development.Crossref | GoogleScholarGoogle Scholar |
Rosenqvist E, Wingsle G, Ögren E (1991) Photoinhibition of photosynthesis in intact willow leaves in response to moderate changes in light and temperature. Physiologia Plantarum 83, 390–396.
| Photoinhibition of photosynthesis in intact willow leaves in response to moderate changes in light and temperature.Crossref | GoogleScholarGoogle Scholar |
Sage RF, Way DA, Kubien DS (2008) Rubisco, Rubisco activase, and global climate change. Journal of Experimental Botany 59, 1581–1595.
| Rubisco, Rubisco activase, and global climate change.Crossref | GoogleScholarGoogle Scholar |
Sato S, Peet MM, Thomas JF (2000) Physiological factors limit fruit set of tomato (Lycopersicon esculentum Mill.) under chronic, mild heat stress. Plant, Cell & Environment 23, 719–726.
| Physiological factors limit fruit set of tomato (Lycopersicon esculentum Mill.) under chronic, mild heat stress.Crossref | GoogleScholarGoogle Scholar |
Sharma DK, Andersen SB, Ottosen C-O, Rosenqvist E (2012) Phenotyping of wheat cultivars for heat tolerance using chlorophyll a fluorescence. Functional Plant Biology 39, 936–947.
| Phenotyping of wheat cultivars for heat tolerance using chlorophyll a fluorescence.Crossref | GoogleScholarGoogle Scholar |
Sharma DK, Andersen SB, Ottosen C-O, Rosenqvist E (2015) Wheat cultivars selected for high F v/F m under heat stress maintain high photosynthesis, total chlorophyll, stomatal conductance, transpiration and dry matter. Physiologia Plantarum 153, 284–298.
| Wheat cultivars selected for high F v/F m under heat stress maintain high photosynthesis, total chlorophyll, stomatal conductance, transpiration and dry matter.Crossref | GoogleScholarGoogle Scholar |
Sita K, Sehgal A, HanumanthaRao B, Nair RM, Vara Prasad PV, Kumar S, Gaur PM, Farroq M, Siddique KHM, Varshney RK, Nayyar H (2017) Food legumes and rising temperatures: effects, adaptive functional mechanisms specific to reproductive growth stage and strategies to improve heat tolerance. Frontiers in Plant Science 8, 1658
| Food legumes and rising temperatures: effects, adaptive functional mechanisms specific to reproductive growth stage and strategies to improve heat tolerance.Crossref | GoogleScholarGoogle Scholar |
Venema JH, Linger P, Van Heusden AW, Van Hasselt PR, Brüggemann W (2005) The inheritance of chilling tolerance in tomato (Lycopersicon spp.). Plant Biology 7, 118–130.
| The inheritance of chilling tolerance in tomato (Lycopersicon spp.).Crossref | GoogleScholarGoogle Scholar |
Vijayalakshmi K, Fritz AK, Paulsen GM, Bai G, Pandravada S, Gill BS (2010) Modeling and mapping QTL for senescence-related traits in winter wheat under high temperature. Molecular Breeding 26, 163–175.
| Modeling and mapping QTL for senescence-related traits in winter wheat under high temperature.Crossref | GoogleScholarGoogle Scholar |
Vollenweider P, Günthardt-Goerg MS (2005) Diagnosis of abiotic and biotic stress factors using the visible symptoms in foliage. Environmental Pollution 137, 455–465.
| Diagnosis of abiotic and biotic stress factors using the visible symptoms in foliage.Crossref | GoogleScholarGoogle Scholar |
Wahid A, Gelani S, Ashraf M, Foolad MR (2007) Heat tolerance in plants: an overview. Environmental and Experimental Botany 61, 199–223.
| Heat tolerance in plants: an overview.Crossref | GoogleScholarGoogle Scholar |
Willits DH, Peet MM (2001) Measurement of chlorophyll fluorescence as a heat stress indicator in tomato: laboratory and greenhouse comparisons. Journal of the American Society for Horticultural Science 126, 188–194.
Wollenweber B, Porter JR, Schellberg J (2003) Lack of interaction between extreme high-temperature events at vegetative and reproductive growth stages in wheat. Journal Agronomy & Crop Science 189, 142–150.
| Lack of interaction between extreme high-temperature events at vegetative and reproductive growth stages in wheat.Crossref | GoogleScholarGoogle Scholar |
Yin Y, Li S, Liao W, Lu Q, Wen X, Lu C (2010) Photosystem II photochemistry, photoinhibition, and the xanthophyll cycle in heat-stressed rice leaves. Journal of Plant Physiology 167, 959–966.
| Photosystem II photochemistry, photoinhibition, and the xanthophyll cycle in heat-stressed rice leaves.Crossref | GoogleScholarGoogle Scholar |
Zhang J, Jiang XD, Li TL, Cao XJ (2014) Photosynthesis and ultrastructure of photosynthetic apparatus in tomato leaves under elevated temperature. Photosynthetica 52, 430–436.
| Photosynthesis and ultrastructure of photosynthetic apparatus in tomato leaves under elevated temperature.Crossref | GoogleScholarGoogle Scholar |
Zhou R, Yu X, Kjær KH, Rosenqvist E, Ottosen C-O, Wu Z (2015) Screening and validation of tomato genotypes under heat stress using F v/F m to reveal the physiological mechanism of heat tolerance. Environmental and Experimental Botany 118, 1–11.
| Screening and validation of tomato genotypes under heat stress using F v/F m to reveal the physiological mechanism of heat tolerance.Crossref | GoogleScholarGoogle Scholar |
Zhou R, Kjaer KH, Rosenqvist E, Yu X, Wu Z, Ottosen C-O (2016) Physiological response to heat stress during seedling and anthesis stage in tomato genotypes differing in heat tolerance. Journal Agronomy & Crop Science 203, 68–80.
| Physiological response to heat stress during seedling and anthesis stage in tomato genotypes differing in heat tolerance.Crossref | GoogleScholarGoogle Scholar |
Zhou R, Kong L, Wu Z, Rosenqvist E, Wang Y, Zhao L, Zhao T, Ottosen C-O (2018) Physiological response of tomatoes at drought, heat and their combination followed by recovery. Physiologia Plantarum
| Physiological response of tomatoes at drought, heat and their combination followed by recovery.Crossref | GoogleScholarGoogle Scholar |
Zinn KE, Tunc-Ozdemir M, Harper JF (2010) Temperature stress and plant sexual reproduction: uncovering the weakest links. Journal of Experimental Botany 61, 1959–1968.
| Temperature stress and plant sexual reproduction: uncovering the weakest links.Crossref | GoogleScholarGoogle Scholar |
